Endoplasmic reticulum stress in obesity and obesity-related disorders: An expanded view

Metabolism: Clinical and Experimental

Volumn 65, Issue 9, 2016, Pages 1238-1246

  Pagliassotti, Michael J ^a   Kim, Paul Y ^b   Estrada, Andrea L ^a   Stewart, Claire M ^a   Gentile, Christopher L ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b GRAMBLING STATE UNIVERSITY   (United States)

Author keywords

Liver; Non alcoholic fatty liver disease; Unfolded protein response

Indexed keywords

FATTY ACID;

ARTICLE; CELL INTERACTION; ENDOPLASMIC RETICULUM MEMBRANE; ENDOPLASMIC RETICULUM STRESS; HUMAN; NONHUMAN; OBESITY; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN PROCESSING; UNFOLDED PROTEIN RESPONSE; ANIMAL; COMPLICATION; METABOLISM; NONALCOHOLIC FATTY LIVER; PATHOPHYSIOLOGY;

ANIMALS; ENDOPLASMIC RETICULUM STRESS; HUMANS; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; UNFOLDED PROTEIN RESPONSE;

EID: 84971631144     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2016.05.002     Document Type: Review

References (111)

1. J. Lee, and U. Ozcan Unfolded protein response signaling and metabolic diseases J Biol Chem 289 2014 1203 1211
2. G.S. Hotamisligil Endoplasmic reticulum stress and the inflammatory basis of metabolic disease Cell 140 2010 900 917
3. U. Ozcan, Q. Cao, E. Yilmaz, A.H. Lee, N.N. Iwakoshi, E. Ozdelen, and et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes Science 306 2004 457 461
4. D. Wang, Y. Wei, and M.J. Pagliassotti Saturated fatty acids promote endoplasmic reticulum stress and liver injury in rats with hepatic steatosis Endocrinology 147 2006 943 951
5. G. Boden, X. Duan, C. Homko, E.J. Molina, W. Song, O. Perez, and et al. Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals Diabetes 57 2008 2438 2444
6. M.F. Gregor, L. Yang, E. Fabbrini, B.S. Mohammed, J.C. Eagon, G.S. Hotamisligil, and et al. Endoplasmic reticulum stress is reduced in tissues of obese subjects after weight loss Diabetes 58 2009 693 700
7. P. Puri, F. Mirshahi, O. Cheung, R. Natarajan, J.W. Maher, J.M. Kellum, and et al. Activation and dysregulation of the unfolded protein response in nonalcoholic fatty liver disease Gastroenterology 134 2008 568 576
8. N.K. Sharma, S.K. Das, A.K. Mondal, O.G. Hackney, W.S. Chu, P.A. Kern, and et al. Endoplasmic reticulum stress markers are associated with obesity in nondiabetic subjects J Clin Endocrinol Metab 93 2008 4532 4541
9. S. Gawrieh, T.M. Baye, M. Carless, J. Wallace, R. Komorowski, D.E. Kleiner, and et al. Hepatic gene networks in morbidly obese patients with nonalcoholic fatty liver disease Obes Surg 20 2010 1698 1709
10. G. van Meer, D.R. Voelker, and G.W. Feigenson Membrane lipids: Where they are and how they behave Nat Rev Mol Cell Biol 9 2008 112 124
11. P. Fagone, and S. Jackowski Membrane phospholipid synthesis and endoplasmic reticulum function J Lipid Res 50 2009 S311 S316 [Suppl.]
12. R.E. Soccio, and J.L. Breslow Intracellular cholesterol transport Arterioscler Thromb Vasc Biol 24 2004 1150 1160
13. M. Schroder, and R.J. Kaufman ER stress and the unfolded protein response Mutat Res 569 2005 29 63
14. G.N. Demartino, and T.G. Gillette Proteasomes: Machines for all reasons Cell 129 2007 659 662
15. A. Hershko, and A. Ciechanover The ubiquitin system Annu Rev Biochem 67 1998 425 479
16. D.T. Rutkowski, and R.S. Hegde Regulation of basal cellular physiology by the homeostatic unfolded protein response J Cell Biol 189 2010 783 794
17. D.T. Rutkowski, and R.J. Kaufman A trip to the ER: Coping with stress Trends Cell Biol 14 2004 20 28
18. K.T. Pfaffenbach, and A.S. Lee The critical role of GRP78 in physiologic and pathologic stress Curr Opin Cell Biol 23 2011 150 156
19. R.J. Kaufman Orchestrating the unfolded protein response in health and disease J Clin Invest 110 2002 1389 1398
20. M. Schroder, and R.J. Kaufman The mammalian unfolded protein response Annu Rev Biochem 74 2005 739 789
21. J. Hollien, and J.S. Weissman Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response Science 313 2006 104 107
22. J. Hollien, J.H. Lin, H. Li, N. Stevens, P. Walter, and J.S. Weissman Regulated Ire1-dependent decay of messenger RNAs in mammalian cells J Cell Biol 186 2009 323 331
23. D.W. Reid, Q. Chen, A.S. Tay, S. Shenolikar, and C.V. Nicchitta The unfolded protein response triggers selective mRNA release from the endoplasmic reticulum Cell 158 2014 1362 1374
24. J. Wu, and R.J. Kaufman From acute ER stress to physiological roles of the unfolded protein response Cell Death Differ 2006
25. R.J. Kaufman Stress signaling from the lumen of the endoplasmic reticulum: Coordination of gene transcriptional and translational controls Genes Dev 13 1999 1211 1233
26. D. Scheuner, B. Song, E. McEwen, C. Liu, R. Laybutt, P. Gillespie, and et al. Translational control is required for the unfolded protein response and in vivo glucose homeostasis Mol Cell 7 2001 1165 1176
27. A.H. Lee, E.F. Scapa, D.E. Cohen, and L.H. Glimcher Regulation of hepatic lipogenesis by the transcription factor XBP1 Science 320 2008 1492 1496
28. R. Sriburi, S. Jackowski, K. Mori, and J.W. Brewer XBP1: A link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum J Cell Biol 167 2004 35 41
29. C.L. Gentile, M. Frye, and M.J. Pagliassotti Endoplasmic reticulum stress and the unfolded protein response in nonalcoholic fatty liver disease Antioxid Redox Signal 15 2011 505 521
30. M.J. Pagliassotti Endoplasmic reticulum stress in nonalcoholic fatty liver disease Annu Rev Nutr 32 2012 17 33
31. C. Hetz The unfolded protein response: Controlling cell fate decisions under ER stress and beyond Nat Rev Mol Cell Biol 13 2012 89 102
32. K. Zhang, and R.J. Kaufman The unfolded protein response: A stress signaling pathway critical for health and disease Neurology 66 2006 S102 S109
33. T. Nakamura, M. Furuhashi, P. Li, H. Cao, G. Tuncman, N. Sonenberg, and et al. Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis Cell 140 2010 338 348
34. O.A. Youssef, S.A. Safran, T. Nakamura, D.A. Nix, G.S. Hotamisligil, and B.L. Bass Potential role for snoRNAs in PKR activation during metabolic stress Proc Natl Acad Sci U S A 112 2015 5023 5028
35. T. Nakamura, R.C. Kunz, C. Zhang, T. Kimura, C.L. Yuan, B. Baccaro, and et al. A critical role for PKR complexes with TRBP in immunometabolic regulation and eIF2alpha phosphorylation in obesity Cell Rep 11 2015 295 307
36. C.I. Michel, C.L. Holley, B.S. Scruggs, R. Sidhu, R.T. Brookheart, L.L. Listenberger, and et al. Small nucleolar RNAs U32a, U33, and U35a are critical mediators of metabolic stress Cell Metab 14 2011 33 44
37. B.S. Scruggs, C.I. Michel, D.S. Ory, and J.E. Schaffer SmD3 regulates intronic noncoding RNA biogenesis Mol Cell Biol 32 2012 4092 4103
38. F. Guo, and D.R. Cavener The GCN2 eIF2alpha kinase regulates fatty-acid homeostasis in the liver during deprivation of an essential amino acid Cell Metab 5 2007 103 114
39. R.J. Kaufman Stress signaling from the lumen of the endoplasmic reticulum: Coordination of gene transcriptional and translational controls Genes Dev 13 1999 1211 1233
40. C.L. Gentile, and M.J. Pagliassotti The endoplasmic reticulum as a potential therapeutic target in nonalcoholic fatty liver disease Curr Opin Investig Drugs 9 2008 1084 1088
41. W.J. Welch, and C.R. Brown Influence of molecular and chemical chaperones on protein folding Cell Stress Chaperones 1 1996 109 115
42. T. Kolter, and M. Wendeler Chemical chaperones - a new concept in drug research Chembiochem 4 2003 260 264
43. C.R. Brown, L.Q. Hong-Brown, J. Biwersi, A.S. Verkman, and W.J. Welch Chemical chaperones correct the mutant phenotype of the delta F508 cystic fibrosis transmembrane conductance regulator protein Cell Stress Chaperones 1 1996 117 125
44. J.A. Burrows, L.K. Willis, and D.H. Perlmutter Chemical chaperones mediate increased secretion of mutant alpha 1-antitrypsin (alpha 1-AT) Z: A potential pharmacological strategy for prevention of liver injury and emphysema in alpha 1-AT deficiency Proc Natl Acad Sci U S A 97 2000 1796 1801
45. Q. Xie, V.I. Khaoustov, C.C. Chung, J. Sohn, B. Krishnan, D.E. Lewis, and et al. Effect of tauroursodeoxycholic acid on endoplasmic reticulum stress-induced caspase-12 activation Hepatology 36 2002 592 601
46. T.W. Loo, and D.M. Clarke Chemical and pharmacological chaperones as new therapeutic agents Expert Rev Mol Med 9 2007 1 18
47. H. Wei, S.J. Kim, Z. Zhang, P.C. Tsai, K.E. Wisniewski, and A.B. Mukherjee ER and oxidative stresses are common mediators of apoptosis in both neurodegenerative and non-neurodegenerative lysosomal storage disorders and are alleviated by chemical chaperones Hum Mol Genet 17 2008 469 477
48. G. Alpini, N. Kanno, J.L. Phinizy, S. Glaser, H. Francis, S. Taffetani, and et al. Tauroursodeoxycholate inhibits human cholangiocarcinoma growth via Ca2 +-, PKC-, and MAPK-dependent pathways Am J Physiol Gastrointest Liver Physiol 286 2004 G973 G982
49. S.F. de Almeida, G. Picarote, J.V. Fleming, M. Carmo-Fonseca, J.E. Azevedo, and M. de Sousa Chemical chaperones reduce endoplasmic reticulum stress and prevent mutant HFE aggregate formation J Biol Chem 282 2007 27905 27912
50. U. Ozcan, E. Yilmaz, L. Ozcan, M. Furuhashi, E. Vaillancourt, R.O. Smith, and et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes Science 313 2006 1137 1140
51. G. Boden, W. Song, X. Duan, P. Cheung, K. Kresge, C. Barrero, and et al. Infusion of glucose and lipids at physiological rates causes acute endoplasmic reticulum stress in rat liver Obesity (Silver Spring) 19 2011 1366 1373
52. A.M. Nivala, L. Reese, M. Frye, C.L. Gentile, and M.J. Pagliassotti Fatty acid-mediated endoplasmic reticulum stress in vivo: Differential response to the infusion of soybean and lard oil in rats Metabolism 62 2013 753 760
53. K.T. Pfaffenbach, C.L. Gentile, A.M. Nivala, D. Wang, Y. Wei, and M.J. Pagliassotti Linking endoplasmic reticulum stress to cell death in hepatocytes: Roles of C/EBP homologous protein and chemical chaperones in palmitate-mediated cell death Am J Physiol Endocrinol Metab 298 2010 E1027 E1035
54. T. Ota, C. Gayet, and H.N. Ginsberg Inhibition of apolipoprotein B100 secretion by lipid-induced hepatic endoplasmic reticulum stress in rodents J Clin Invest 118 2008 316 332
55. H.L. Kammoun, H. Chabanon, I. Hainault, S. Luquet, C. Magnan, T. Koike, and et al. GRP78 expression inhibits insulin and ER stress-induced SREBP-1c activation and reduces hepatic steatosis in mice J Clin Invest 119 2009 1201 1215
56. R. Ye, D.Y. Jung, J.Y. Jun, J. Li, S. Luo, H.J. Ko, and et al. Grp78 heterozygosity promotes adaptive unfolded protein response and attenuates diet-induced obesity and insulin resistance Diabetes 59 2010 6 16
57. S.R. Anderson, D.A. Gilge, A.L. Steiber, and S.F. Previs Diet-induced obesity alters protein synthesis: Tissue-specific effects in fasted versus fed mice Metabolism 57 2008 347 354
58. S. Fu, J. Fan, J. Blanco, A. Gimenez-Cassina, N.N. Danial, S.M. Watkins, and et al. Polysome profiling in liver identifies dynamic regulation of endoplasmic reticulum translatome by obesity and fasting PLoS Genet 8 2012 e1002902
59. M. Hatanaka, B. Maier, E.K. Sims, A.T. Templin, R.N. Kulkarni, C. Evans-Molina, and et al. Palmitate induces mRNA translation and increases ER protein load in islet beta-cells via activation of the mammalian target of rapamycin pathway Diabetes 63 2014 3404 3415
60. L. Khamzina, A. Veilleux, S. Bergeron, and A. Marette Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle of obese rats: Possible involvement in obesity-linked insulin resistance Endocrinology 146 2005 1473 1481
61. D. Burdakov, O.H. Petersen, and A. Verkhratsky Intraluminal calcium as a primary regulator of endoplasmic reticulum function Cell Calcium 38 2005 303 310
62. A. Gorlach, P. Klappa, and T. Kietzmann The endoplasmic reticulum: Folding, calcium homeostasis, signaling, and redox control Antioxid Redox Signal 8 2006 1391 1418
63. A. Zarain-Herzberg, and G. Alvarez-Fernandez Sarco(endo)plasmic reticulum Ca2 +-ATPase-2 gene: Structure and transcriptional regulation of the human gene ScientificWorldJournal 2 2002 1469 1483
64. S.W. Park, Y. Zhou, J. Lee, J. Lee, and U. Ozcan Sarco(endo)plasmic reticulum Ca2 +-ATPase 2b is a major regulator of endoplasmic reticulum stress and glucose homeostasis in obesity Proc Natl Acad Sci U S A 107 2010 19320 19325
65. S. Fu, L. Yang, P. Li, O. Hofmann, L. Dicker, W. Hide, and et al. Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity Nature 473 2011 528 531
66. T. Hartley, J. Brumell, and A. Volchuk Emerging roles for the ubiquitin-proteasome system and autophagy in pancreatic beta-cells Am J Physiol Endocrinol Metab 296 2009 E1 10
67. T. Otoda, T. Takamura, H. Misu, T. Ota, S. Murata, H. Hayashi, and et al. Proteasome dysfunction mediates obesity-induced endoplasmic reticulum stress and insulin resistance in the liver Diabetes 62 2013 811 824
68. J.H. Moffitt, B.A. Fielding, R. Evershed, R. Berstan, J.M. Currie, and A. Clark Adverse physicochemical properties of tripalmitin in beta cells lead to morphological changes and lipotoxicity in vitro Diabetologia 48 2005 1819 1829
69. N.M. Borradaile, X. Han, J.D. Harp, S.E. Gale, D.S. Ory, and J.E. Schaffer Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death J Lipid Res 47 2006 2726 2737
70. L. Abrami, B. Kunz, I. Iacovache, and F.G. van der Goot Palmitoylation and ubiquitination regulate exit of the Wnt signaling protein LRP6 from the endoplasmic reticulum Proc Natl Acad Sci U S A 105 2008 5384 5389
71. E.M. Lynes, M. Bui, M.C. Yap, M.D. Benson, B. Schneider, L. Ellgaard, and et al. Palmitoylated TMX and calnexin target to the mitochondria-associated membrane EMBO J 31 2012 457 470
72. R.F. Thorne, K.J. Ralston, C.E. de Bock, N.M. Mhaidat, X.D. Zhang, A.W. Boyd, and et al. Palmitoylation of CD36/FAT regulates the rate of its post-transcriptional processing in the endoplasmic reticulum Biochim Biophys Acta 2010 1803 1298 1307
73. A.C. Baldwin, C.D. Green, L.K. Olson, M.A. Moxley, and J.A. Corbett A role for aberrant protein palmitoylation in FFA-induced ER stress and beta-cell death Am J Physiol Endocrinol Metab 302 2012 E1390 E1398
74. M.E. Linder, and R.J. Deschenes Palmitoylation: Policing protein stability and traffic Nat Rev Mol Cell Biol 8 2007 74 84
75. J. Greaves, and L.H. Chamberlain Palmitoylation-dependent protein sorting J Cell Biol 176 2007 249 254
76. W. Ren, U.S. Jhala, and K. Du Proteomic analysis of protein palmitoylation in adipocytes Adipocyte 2 2013 17 28
77. D.B. Williams Beyond lectins: The calnexin/calreticulin chaperone system of the endoplasmic reticulum J Cell Sci 119 2006 615 623
78. E.M. Lynes, A. Raturi, M. Shenkman, C. Ortiz Sandoval, M.C. Yap, J. Wu, and et al. Palmitoylation is the switch that assigns calnexin to quality control or ER Ca2 + signaling J Cell Sci 126 2013 3893 3903
79. L. Liscum, and N.J. Munn Intracellular cholesterol transport Biochim Biophys Acta 1438 1999 19 37
80. Y. Lange, J. Ye, M. Rigney, and T.L. Steck Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol J Lipid Res 40 1999 2264 2270
81. R. Ross Cell biology of atherosclerosis Annu Rev Physiol 57 1995 791 804
82. Y. Li, M. Ge, L. Ciani, G. Kuriakose, E.J. Westover, M. Dura, and et al. Enrichment of endoplasmic reticulum with cholesterol inhibits sarcoplasmic-endoplasmic reticulum calcium ATPase-2b activity in parallel with increased order of membrane lipids: Implications for depletion of endoplasmic reticulum calcium stores and apoptosis in cholesterol-loaded macrophages J Biol Chem 279 2004 37030 37039
83. Z.Z. Li, M. Berk, T.M. McIntyre, and A.E. Feldstein Hepatic lipid partitioning and liver damage in nonalcoholic fatty liver disease: Role of stearoyl-CoA desaturase J Biol Chem 284 2009 5637 5644
84. T. Promlek, Y. Ishiwata-Kimata, M. Shido, M. Sakuramoto, K. Kohno, and Y. Kimata Membrane aberrancy and unfolded proteins activate the endoplasmic reticulum stress sensor Ire1 in different ways Mol Biol Cell 22 2011 3520 3532
85. R. Volmer, K. van der Ploeg, and D. Ron Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains Proc Natl Acad Sci U S A 110 2013 4628 4633
86. N.S. Hou, A. Gutschmidt, D.Y. Choi, K. Pather, X. Shi, J.L. Watts, and et al. Activation of the endoplasmic reticulum unfolded protein response by lipid disequilibrium without disturbed proteostasis in vivo Proc Natl Acad Sci U S A 111 2014 E2271 E2280
87. H. Ariyama, N. Kono, S. Matsuda, T. Inoue, and H. Arai Decrease in membrane phospholipid unsaturation induces unfolded protein response J Biol Chem 285 2010 22027 22035
88. Y. Kitai, H. Ariyama, N. Kono, D. Oikawa, T. Iwawaki, and H. Arai Membrane lipid saturation activates IRE1alpha without inducing clustering Genes Cells 18 2013 798 809
89. G. Thibault, G. Shui, W. Kim, G.C. McAlister, N. Ismail, S.P. Gygi, and et al. The membrane stress response buffers lethal effects of lipid disequilibrium by reprogramming the protein homeostasis network Mol Cell 48 2012 16 27
90. M. Lebiedzinska, G. Szabadkai, A.W. Jones, J. Duszynski, and M.R. Wieckowski Interactions between the endoplasmic reticulum, mitochondria, plasma membrane and other subcellular organelles Int J Biochem Cell Biol 41 2009 1805 1816
91. A.A. Rowland, and G.K. Voeltz Endoplasmic reticulum-mitochondria contacts: Function of the junction Nat Rev Mol Cell Biol 13 2012 607 625
92. T.K. Rainbolt, J.M. Saunders, and R.L. Wiseman Stress-responsive regulation of mitochondria through the ER unfolded protein response Trends Endocrinol Metab 25 2014 528 537
93. R. Bravo, J.M. Vicencio, V. Parra, R. Troncoso, J.P. Munoz, M. Bui, and et al. Increased ER-mitochondrial coupling promotes mitochondrial respiration and bioenergetics during early phases of ER stress J Cell Sci 124 2011 2143 2152
94. J.H. Lim, H.J. Lee, M. Ho Jung, and J. Song Coupling mitochondrial dysfunction to endoplasmic reticulum stress response: A molecular mechanism leading to hepatic insulin resistance Cell Signal 21 2009 169 177
95. D.G. Brdiczka, D.B. Zorov, and S.S. Sheu Mitochondrial contact sites: Their role in energy metabolism and apoptosis Biochim Biophys Acta 2006 1762 148 163
96. J.E. Vance Phospholipid synthesis and transport in mammalian cells Traffic 16 2015 1 18
97. J.E. Vance MAM (mitochondria-associated membranes) in mammalian cells: Lipids and beyond Biochim Biophys Acta 2014 1841 595 609
98. J.R. Friedman, B.M. Webster, D.N. Mastronarde, K.J. Verhey, and G.K. Voeltz ER sliding dynamics and ER-mitochondrial contacts occur on acetylated microtubules J Cell Biol 190 2010 363 375
99. G. Marino, F. Pietrocola, T. Eisenberg, Y. Kong, S.A. Malik, A. Andryushkova, and et al. Regulation of autophagy by cytosolic acetyl-coenzyme A Mol Cell 53 2014 710 725
100. A.M. Davenport, L.N. Collins, H. Chiu, P.J. Minor, P.W. Sternberg, and A. Hoelz Structural and functional characterization of the alpha-tubulin acetyltransferase MEC-17 J Mol Biol 426 2014 2605 2616
101. A. Szyk, A.M. Deaconescu, J. Spector, B. Goodman, M.L. Valenstein, N.E. Ziolkowska, and et al. Molecular basis for age-dependent microtubule acetylation by tubulin acetyltransferase Cell 157 2014 1405 1415
102. N.R. Bertos, B. Gilquin, G.K. Chan, T.J. Yen, S. Khochbin, and X.J. Yang Role of the tetradecapeptide repeat domain of human histone deacetylase 6 in cytoplasmic retention J Biol Chem 279 2004 48246 48254
103. B.J. North, B.L. Marshall, M.T. Borra, J.M. Denu, and E. Verdin The human Sir2 ortholog, SIRT2, is an NAD +-dependent tubulin deacetylase Mol Cell 11 2003 437 444
104. D. Perdiz, R. Mackeh, C. Pous, and A. Baillet The ins and outs of tubulin acetylation: More than just a post-translational modification? Cell Signal 23 2011 763 771
105. Y. Zhang, N. Li, C. Caron, G. Matthias, D. Hess, S. Khochbin, and et al. HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo EMBO J 22 2003 1168 1179
106. N. Narayan, I.H. Lee, R. Borenstein, J. Sun, R. Wong, G. Tong, and et al. The NAD-dependent deacetylase SIRT2 is required for programmed necrosis Nature 492 2012 199 204
107. H.J. Kim, Y. Nagano, S.J. Choi, S.Y. Park, H. Kim, T.P. Yao, and et al. HDAC6 maintains mitochondrial connectivity under hypoxic stress by suppressing MARCH5/MITOL dependent MFN2 degradation Biochem Biophys Res Commun 464 2015 1235 1240
108. D. Wang, Q. Meng, L. Huo, M. Yang, L. Wang, X. Chen, and et al. Overexpression of Hdac6 enhances resistance to virus infection in embryonic stem cells and in mice Protein Cell 6 2015 152 156
109. A.P. Arruda, B.M. Pers, G. Parlakgul, E. Guney, K. Inouye, and G.S. Hotamisligil Chronic enrichment of hepatic endoplasmic reticulum-mitochondria contact leads to mitochondrial dysfunction in obesity Nat Med 20 2014 1427 1435
110. E. Tubbs, P. Theurey, G. Vial, N. Bendridi, A. Bravard, M.A. Chauvin, and et al. Mitochondria-associated endoplasmic reticulum membrane (MAM) integrity is required for insulin signaling and is implicated in hepatic insulin resistance Diabetes 63 2014 3279 3294
111. J.R. Friedman, and G.K. Voeltz The ER in 3D: A multifunctional dynamic membrane network Trends Cell Biol 21 2011 709 717